The VgrG proteins are "à la carte" delivery systems for bacterial type VI effectors

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17872-17884

  Hachani, Abderrahman ^a   Allsopp, Luke P ^a   Oduko, Yewande ^a   Filloux, Alain ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; GENE ENCODING; METABOLITES; PHYSIOLOGY; PROTEINS;

BACTERIAL KILLING; COMPLEMENTATION; DELIVERY SYSTEMS; INDEPENDENT CONTRIBUTIONS; P.AERUGINOSA; PSEUDOMONAS AERUGINOSA; SECRETION SYSTEMS; TOXIC ACTIVITIES;

TOXIC MATERIALS;

BACTERIAL PROTEIN; BACTERIAL TOXIN; CARRIER PROTEINS AND BINDING PROTEINS; NUCLEASE; PA 0099; PROTEIN VGRG; RHS PROTEIN; RHSP1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE; GENETIC CODE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; TYPE IV SECRETION SYSTEM; VGRG1A GENE; VGRG1C GENE;

BACTERIAL CELL ENVELOPE; BACTERIAL GENETICS; BACTERIAL TOXIN; MICROBIOLOGY; PROTEIN TRANSLOCATION; PSEUDOMONAS AERUGINOSA (P. AERUGINOSA); TYPE VI SECRETION SYSTEM; VGRG;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BACTERIAL TOXINS; CARRIER PROTEINS; PSEUDOMONAS AERUGINOSA;

EID: 84903434335     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.563429     Document Type: Article

References (66)

1. Ho, B. T., Dong, T. G., and Mekalanos, J. J. (2014) A view to a kill: the bacterial type VI secretion system. Cell Host. Microbe 15, 9-21
2. Russell, A. B., Peterson, S. B., and Mougous, J. D. (2014) Type VI secretion system effectors: poisons with a purpose. Nat. Rev. Microbiol. 12, 137-148
3. Leiman, P. G., Arisaka, F., van Raaij, M. J., Kostyuchenko, V. A., Aksyuk, A. A., Kanamaru, S., and Rossmann, M. G. (2010) Morphogenesis of the T4 tail and tail fibers. Virol. J. 7, 355
4. Mougous, J. D., Cuff, M. E., Raunser, S., Shen, A., Zhou, M., Gifford, C. A., Goodman, A. L., Joachimiak, G., Ordoñez, C. L., Lory, S., Walz, T., Joachimiak, A., and Mekalanos, J. J. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530 (Pubitemid 43865892)
5. Leiman, P. G., Basler, M., Ramagopal, U. A., Bonanno, J. B., Sauder, J. M., Pukatzki, S., Burley, S. K., Almo, S. C., and Mekalanos, J. J. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. U.S.A. 106, 4154-4159
6. Shneider, M. M., Buth, S. A., Ho, B. T., Basler, M., Mekalanos, J. J., and Leiman, P. G. (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500, 350-353
7. Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J., and Mekalanos, J. J. (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483, 182-186
8. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H., and Mogk, A. (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28, 315-325
9. Lossi, N. S., Manoli, E., Förster, A., Dajani, R., Pape, T., Freemont, P., and Filloux, A. (2013) The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. J. Biol. Chem. 288, 7536-7548
10. Zhang, X. Y., Brunet, Y. R., Logger, L., Douzi, B., Cambillau, C., Journet, L., and Cascales, E. (2013) Dissection of the TssB-TssC interface during type VI secretion sheath complex formation. PLoS ONE 8, e81074
11. Basler, M., and Mekalanos, J. J. (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337, 815
12. Kapitein, N., Bönemann, G., Pietrosiuk, A., Seyffer, F., Hausser, I., Locker, J. K., and Mogk, A. (2013) ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol. Microbiol. 87, 1013-1028
13. Kapitein, N., and Mogk, A. (2013) Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition. Curr. Opin. Microbiol. 16, 52-58
14. Pietrosiuk, A., Lenherr, E. D., Falk, S., Bönemann, G., Kopp, J., Zentgraf, H., Sinning, I., and Mogk, A. (2011) Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J. Biol. Chem. 286, 30010-30021
15. Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S., and Lory, S. (2004)Asignaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7, 745-754 (Pubitemid 39462694)
16. Goodman, A. L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A., and Lory, S. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev. 23, 249-259
17. Moscoso, J. A., Mikkelsen, H., Heeb, S., Williams, P., and Filloux, A. (2011) The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ. Microbiol. 13, 3128-3138
18. Brencic, A., and Lory, S. (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol. Microbiol. 72, 612-632
19. Casabona, M. G., Silverman, J. M., Sall, K. M., Boyer, F., Couté, Y., Poirel, J., Grunwald, D., Mougous, J. D., Elsen, S., and Attree, I. (2013) An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa. Environ. Microbiol. 15, 471-486
20. Lossi, N. S., Manoli, E., Simpson, P., Jones, C., Hui, K., Dajani, R., Coulthurst, S. J., Freemont, P., and Filloux, A. (2012) The archetype Pseudomonas aeruginosa proteins TssB and TagJ form a novel sub-complex in the bacterial Type VI secretion system. Mol. Microbiol. 86, 437-456
21. Mougous, J. D., Gifford, C. A., Ramsdell, T. L., and Mekalanos, J. J. (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol. 9, 797-803 (Pubitemid 47019466)
22. Hachani, A., Lossi, N. S., Hamilton, A., Jones, C., Bleves, S., Albesa-Jové, D., and Filloux, A. (2011) Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J. Biol. Chem. 286, 12317-12327
23. Hood, R. D., Singh, P., Hsu, F., Güvener, T., Carl, M. A., Trinidad, R. R., Silverman, J. M., Ohlson, B. B., Hicks, K. G., Plemel, R. L., Li, M., Schwarz, S., Wang, W. Y., Merz, A. J., Goodlett, D. R., and Mougous, J. D. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25-37
24. Russell, A. B., Hood, R. D., Bui, N. K., LeRoux, M., Vollmer, W., and Mougous, J. D. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347
25. Russell, A. B., Singh, P., Brittnacher, M., Bui, N. K., Hood, R. D., Carl, M. A., Agnello, D. M., Schwarz, S., Goodlett, D. R., Vollmer, W., and Mougous, J. D. (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11, 538-549
26. English, G., Trunk, K., Rao, V. A., Srikannathasan, V., Hunter, W. N., and Coulthurst, S. J. (2012) New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens. Mol. Microbiol. 86, 921-936
27. Murdoch, S. L., Trunk, K., English, G., Fritsch, M. J., Pourkarimi, E., and Coulthurst, S. J. (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193, 6057-6069
28. Schwarz, S., Hood, R. D., and Mougous, J. D. (2010) What is type VI secretion doing in all those bugs? Trends Microbiol. 18, 531-537
29. Basler, M., Ho, B. T., and Mekalanos, J. J. (2013) Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152, 884-894
30. Ballister, E. R., Lai, A. H., Zuckermann, R. N., Cheng, Y., and Mougous, J. D. (2008) In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. U.S.A. 105, 3733-3738 (Pubitemid 351723467)
31. Silverman, J. M., Agnello, D. M., Zheng, H., Andrews, B. T., Li, M., Catalano, C. E., Gonen, T., and Mougous, J. D. (2013) Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol. Cell 51, 584-593
32. Brooks, T. M., Unterweger, D., Bachmann, V., Kostiuk, B., and Pukatzki, S. (2013) Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J. Biol. Chem. 288, 7618-7625
33. Dong, T. G., Ho, B. T., Yoder-Himes, D. R., and Mekalanos, J. J. (2013) Identification of T6SS-dependent effector and immunity proteins by Tnseq in Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 110, 2623-2628
34. Hachani, A., Lossi, N. S., and Filloux, A. (2013) A visual assay to monitor T6SS-mediated bacterial competition. J. Vis. Exp. 73, e50103
35. Guzman, L. M., Belin, D., Carson, M. J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130
36. Gotfredsen, M., and Gerdes, K. (1998) The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol. Microbiol. 29, 1065-1076 (Pubitemid 28389446)
37. Vasseur, P., Vallet-Gely, I., Soscia, C., Genin, S., and Filloux, A. (2005) The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151, 985-997 (Pubitemid 40425032)
38. Herrero, M., de Lorenzo, V., and Timmis, K. N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172, 6557-6567 (Pubitemid 20372801)
39. Kaniga, K., Delor, I., and Cornelis, G. R. (1991) A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109, 137-141
40. Figurski, D. H., and Helinski, D. R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U.S.A. 76, 1648-1652 (Pubitemid 9175374)
41. Viarre, V., Cascales, E., Ball, G., Michel, G. P., Filloux, A., and Voulhoux, R. (2009) HxcQ liposecretin is self-piloted to the outer membrane by its N-terminal lipid anchor. J. Biol. Chem. 284, 33815-33823
42. Winsor, G. L., Lam, D. K., Fleming, L., Lo, R., Whiteside, M. D., Yu, N. Y., Hancock, R. E., and Brinkman, F. S. (2011) Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39, D596-D600
43. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
44. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
45. Jackson, A. P., Thomas, G. H., Parkhill, J., and Thomson, N. R. (2009) Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement. BMC Genomics 10, 584
46. Poole, S. J., Diner, E. J., Aoki, S. K., Braaten, B. A., t'Kint de Roodenbeke, C., Low, D. A., and Hayes, C. S. (2011) Identification of functional toxin/ immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet. 7, e1002217
47. Koskiniemi, S., Lamoureux, J. G., Nikolakakis, K. C., t'Kint de Roodenbeke, C., Kaplan, M. D., Low, D. A., and Hayes, C. S. (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc. Natl. Acad. Sci. U.S.A. 110, 7032-7037
48. Zhang, D., de Souza, R. F., Anantharaman, V., Iyer, L. M., and Aravind, L. (2012) Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol. Direct 7, 18
49. Jones, C., Hachani, A., Manoli, E., and Filloux, A. (2014) An rhs gene linked to the second type vi secretion cluster is a feature of the Pseudomonas aeruginosa strain PA14. J. Bacteriol. 196, 800-810
50. Durand, E., Derrez, E., Audoly, G., Spinelli, S., Ortiz-Lombardia, M., Raoult, D., Cascales, E., and Cambillau, C. (2012) Crystal structure of the VgrG1 actin cross-linking domain of the Vibrio cholerae type VI secretion system. J. Biol. Chem. 287, 38190-38199
51. Ma, A. T., McAuley, S., Pukatzki, S., and Mekalanos, J. J. (2009) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5, 234-243
52. Ma, A. T., and Mekalanos, J. J. (2010) In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc. Natl. Acad. Sci. U.S.A. 107, 4365-4370
53. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D., and Mekalanos, J. J. (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U.S.A. 104, 15508-15513 (Pubitemid 47502947)
54. Suarez, G., Sierra, J. C., Erova, T. E., Sha, J., Horneman, A. J., and Chopra, A. K. (2010) A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192, 155-168
55. Filloux, A. (2013) Microbiology: a weapon for bacterial warfare. Nature 500, 284-285
56. Coulthurst, S. J. (2013) The Type VI secretion system: a widespread and versatile cell targeting system. Res. Microbiol. 164, 640-654
57. Whitney, J. C., Chou, S., Russell, A. B., Biboy, J., Gardiner, T. E., Ferrin, M. A., Brittnacher, M., Vollmer, W., and Mougous, J. D. (2013) Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J. Biol. Chem. 288, 26616-26624
58. Russell, A. B., LeRoux, M., Hathazi, K., Agnello, D. M., Ishikawa, T., Wiggins, P. A., Wai, S. N., and Mougous, J. D. (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496, 508-512
59. Bönemann, G., Pietrosiuk, A., and Mogk, A. (2010) Tubules and donuts: a type VI secretion story. Mol. Microbiol. 76, 815-821
60. Cascales, E., and Cambillau, C. (2012) Structural biology of type VI secretion systems. Philos. Trans R Soc. Lond B Biol. Sci. 367, 1102-1111
61. Filloux, A. (2009) The type VI secretion system: a tubular story. EMBO J. 28, 309-310
62. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., Brinkman, F. S., Hufnagle, W. O., Kowalik, D. J., Lagrou, M., Garber, R. L., Goltry, L., Tolentino, E., Westbrock-Wadman, S., Yuan, Y., Brody, L. L., Coulter, S. N., Folger, K. R., Kas, A., Larbig, K., Lim, R., Smith, K., Spencer, D., Wong, G. K., Wu, Z., Paulsen, I. T., Reizer, J., Saier, M. H., Hancock, R. E., Lory, S., and Olson, M. V. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964
63. Wiener, M., Freymann, D., Ghosh, P., and Stroud, R. M. (1997) Crystal structure of colicin Ia. Nature 385, 461-464 (Pubitemid 27065935)
64. Lesic, B., Starkey, M., He, J., Hazan, R., and Rahme, L. G. (2009) Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155, 2845-2855
65. Sana, T. G., Hachani, A., Bucior, I., Soscia, C., Garvis, S., Termine, E., Engel, J., Filloux, A., and Bleves, S. (2012) The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J. Biol. Chem. 287, 27095-27105
66. Ruhe, Z. C., Low, D. A., and Hayes, C. S. (2013) Bacterial contact-dependent growth inhibition. Trends Microbiol. 21, 230-237